Interactions between two parasites of brown trout (Salmo trutta): Consequences of preinfection

Preinfection by one parasitic species may facilitate or by contrast hamper the subsequent penetration and/or establishment of other parasites in a host. The biology of interacting species, timing of preinfection, and dosage of subsequent parasite exposure are likely important variables in this multi...

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Veröffentlicht in:Ecology and evolution 2018-10, Vol.8 (20), p.9986-9997
Hauptverfasser: Gopko, Mikhail, Chowdhury, M. Motiur R., Taskinen, Jouni
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Chowdhury, M. Motiur R.
Taskinen, Jouni
description Preinfection by one parasitic species may facilitate or by contrast hamper the subsequent penetration and/or establishment of other parasites in a host. The biology of interacting species, timing of preinfection, and dosage of subsequent parasite exposure are likely important variables in this multiparasite dynamic infection process. The increased vulnerability to subsequent infection can be an important and often overlooked factor influencing parasite virulence. We investigated how the preinfection by freshwater pearl mussel Margaritifera margaritifera glochidia could influence the success of subsequent infection by the common trematode Diplostomum pseudospathaceum in brown trout Salmo trutta and vice versa whether preinfection by the trematode made fish more susceptible to glochidia infection. The first experiment was repeated twice with different (low and high) exposure doses to initiate the subsequent trematode infection, while in the second experiment we varied the timing of the preinfection with trematodes. The preinfection with glochidia made fish more vulnerable to subsequent infection with trematodes. Since the trematodes penetrate through the gills, we suggest that increased host vulnerability was most likely the result of increased respiration caused by the freshwater pearl mussel glochidia encysted on gills. In turn, brown trout preinfected with trematodes were more vulnerable to the subsequent glochidial infection, but only if they were preinfected shortly before the subsequent infection (20 hr). Fish preinfected with trematodes earlier (2 weeks before the subsequent infection) did not differ in their vulnerability to glochidia. These effects were observed at moderate intensities of infections similar to those that occur in nature. Our study demonstrates how the timing and sequence of exposure to parasitic species can influence infection success in a host–multiparasite system. It indicates that the negative influence of glochidia on host fitness is likely to be underestimated and that this should be taken into consideration when organizing freshwater pearl mussel restoration procedures. Freshwater pearl mussels's parasitic stage (glochidia) is usually considered to be not very harmful to their host, brown trout. However, even a small damage to fish gills caused by this parasite can make its host more vulnerable to subsequent infections. We demonstrate that the glochidia infection predispose fish to the infection by common trematode. Interestin
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The first experiment was repeated twice with different (low and high) exposure doses to initiate the subsequent trematode infection, while in the second experiment we varied the timing of the preinfection with trematodes. The preinfection with glochidia made fish more vulnerable to subsequent infection with trematodes. Since the trematodes penetrate through the gills, we suggest that increased host vulnerability was most likely the result of increased respiration caused by the freshwater pearl mussel glochidia encysted on gills. In turn, brown trout preinfected with trematodes were more vulnerable to the subsequent glochidial infection, but only if they were preinfected shortly before the subsequent infection (20 hr). Fish preinfected with trematodes earlier (2 weeks before the subsequent infection) did not differ in their vulnerability to glochidia. These effects were observed at moderate intensities of infections similar to those that occur in nature. 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Motiur R.</creatorcontrib><creatorcontrib>Taskinen, Jouni</creatorcontrib><title>Interactions between two parasites of brown trout (Salmo trutta): Consequences of preinfection</title><title>Ecology and evolution</title><addtitle>Ecol Evol</addtitle><description>Preinfection by one parasitic species may facilitate or by contrast hamper the subsequent penetration and/or establishment of other parasites in a host. The biology of interacting species, timing of preinfection, and dosage of subsequent parasite exposure are likely important variables in this multiparasite dynamic infection process. The increased vulnerability to subsequent infection can be an important and often overlooked factor influencing parasite virulence. We investigated how the preinfection by freshwater pearl mussel Margaritifera margaritifera glochidia could influence the success of subsequent infection by the common trematode Diplostomum pseudospathaceum in brown trout Salmo trutta and vice versa whether preinfection by the trematode made fish more susceptible to glochidia infection. The first experiment was repeated twice with different (low and high) exposure doses to initiate the subsequent trematode infection, while in the second experiment we varied the timing of the preinfection with trematodes. The preinfection with glochidia made fish more vulnerable to subsequent infection with trematodes. Since the trematodes penetrate through the gills, we suggest that increased host vulnerability was most likely the result of increased respiration caused by the freshwater pearl mussel glochidia encysted on gills. 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Motiur R.</au><au>Taskinen, Jouni</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Interactions between two parasites of brown trout (Salmo trutta): Consequences of preinfection</atitle><jtitle>Ecology and evolution</jtitle><addtitle>Ecol Evol</addtitle><date>2018-10</date><risdate>2018</risdate><volume>8</volume><issue>20</issue><spage>9986</spage><epage>9997</epage><pages>9986-9997</pages><issn>2045-7758</issn><eissn>2045-7758</eissn><abstract>Preinfection by one parasitic species may facilitate or by contrast hamper the subsequent penetration and/or establishment of other parasites in a host. The biology of interacting species, timing of preinfection, and dosage of subsequent parasite exposure are likely important variables in this multiparasite dynamic infection process. The increased vulnerability to subsequent infection can be an important and often overlooked factor influencing parasite virulence. 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In turn, brown trout preinfected with trematodes were more vulnerable to the subsequent glochidial infection, but only if they were preinfected shortly before the subsequent infection (20 hr). Fish preinfected with trematodes earlier (2 weeks before the subsequent infection) did not differ in their vulnerability to glochidia. These effects were observed at moderate intensities of infections similar to those that occur in nature. Our study demonstrates how the timing and sequence of exposure to parasitic species can influence infection success in a host–multiparasite system. It indicates that the negative influence of glochidia on host fitness is likely to be underestimated and that this should be taken into consideration when organizing freshwater pearl mussel restoration procedures. Freshwater pearl mussels's parasitic stage (glochidia) is usually considered to be not very harmful to their host, brown trout. However, even a small damage to fish gills caused by this parasite can make its host more vulnerable to subsequent infections. We demonstrate that the glochidia infection predispose fish to the infection by common trematode. Interestingly, fish preinfected with trematode was also more vulnerable to infection with glochidia, but only, if preinfection happened shortly before the second infection.</abstract><cop>England</cop><pub>John Wiley &amp; Sons, Inc</pub><pmid>30397441</pmid><doi>10.1002/ece3.4406</doi><tpages>12</tpages><orcidid>https://orcid.org/0000-0002-1525-6557</orcidid><oa>free_for_read</oa></addata></record>
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source Wiley Online Library Open Access; DOAJ Directory of Open Access Journals; Wiley Online Library Journals Frontfile Complete; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central
subjects community ecology
Diplostomum
experimental infection
Exposure
Fish
Fitness
freshwater pearl mussel
Gills
host–parasite interactions
Infections
Mollusks
multiple infections
Original Research
Parasites
Restoration
Salmo trutta
Species
Trout
Virulence
title Interactions between two parasites of brown trout (Salmo trutta): Consequences of preinfection
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